Host-mediated, cross-generational intraspecific competition in a herbivore species

10.24072/pcjournal.49 - Peer Community Journal, Volume 1 (2021), article no. e61.

Get full text PDF Peer reviewed and recommended by PCI

Conspecific insect herbivores co-occurring on the same host plant interact both directly through interference competition and indirectly through exploitative competition, plant-mediated interactions and enemy-mediated interactions. However, the situation is less clear when the interactions between conspecific insect herbivores are separated in time within the same growing season, as it is the case for multivoltine species. We hypothesized that early season herbivory would result in reduced egg laying and reduced performance of the next generation of herbivores on previously attacked plants. We tested this hypothesis in a choice experiment with box tree moth females (Cydalima perspectalis Walker, Lepidoptera: Crambidae). These females were exposed to box trees (Buxus sempervirens L., Buxaceae) that were either undamaged or attacked by conspecific larvae earlier in the season. We then compared the performance of the next generation larvae on previously damaged vs undamaged plants. Previous herbivory had no effect on oviposition behaviour, but the weight of next generation larvae was significantly lower in previously damaged plants. There was a negative correlation between the number of egg clutches laid on plants by the first generation and the performance of the next generation larvae. Overall, our findings reveal that early season herbivory reduces the performance of conspecific individuals on the same host plant later in the growing season, and that this time-lagged intraspecific competition results from a mismatch between the oviposition preference of females and the performance of its offspring.

Published online:
DOI: 10.24072/pcjournal.49
Castagneyrol, Bastien 1; van Halder, Inge 1; Kadiri, Yasmine 1; Schillé, Laura 1; Jactel, Hervé 1

1 BIOGECO, Univ. Bordeaux - INRAE, F-33612 Cestas, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights
     author = {Castagneyrol, Bastien and van Halder, Inge and Kadiri, Yasmine and Schill\'e, Laura and Jactel, Herv\'e},
     title = {Host-mediated, cross-generational intraspecific competition in a herbivore species},
     journal = {Peer Community Journal},
     eid = {e61},
     publisher = {Peer Community In},
     volume = {1},
     year = {2021},
     doi = {10.24072/pcjournal.49},
     url = {}
TI  - Host-mediated, cross-generational intraspecific competition in a herbivore species
JO  - Peer Community Journal
PY  - 2021
DA  - 2021///
VL  - 1
PB  - Peer Community In
UR  -
UR  -
DO  - 10.24072/pcjournal.49
ID  - 10_24072_pcjournal_49
ER  - 
%0 Journal Article
%T Host-mediated, cross-generational intraspecific competition in a herbivore species
%J Peer Community Journal
%D 2021
%V 1
%I Peer Community In
%R 10.24072/pcjournal.49
%F 10_24072_pcjournal_49
Castagneyrol, Bastien; van Halder, Inge; Kadiri, Yasmine; Schillé, Laura; Jactel, Hervé. Host-mediated, cross-generational intraspecific competition in a herbivore species. Peer Community Journal, Volume 1 (2021), article  no. e61. doi : 10.24072/pcjournal.49.

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100072

[1] Abdala‐Roberts, L.; Reyes‐Hernández, M.; Quijano‐Medina, T.; Moreira, X.; Francisco, M.; Angulo, D. F.; Parra‐Tabla, V.; Virgen, A.; Rojas, J. C. Effects of amount and recurrence of leaf herbivory on the induction of direct and indirect defences in wild cotton, Plant Biology, Volume 21 (2019) no. 6, pp. 1063-1071 | DOI

[2] Agrawal, A. A. Induced responses to herbivory in wild radish: effects on several herbivores and plant fitness, Ecology, Volume 80 (1999) no. 5, pp. 1713-1723 | DOI

[3] Alkan Akıncı, H.; Kurdoğlu, O. Damage Level of Cydalima perspectalis (Lepidoptera: Crambidae) on Naturally Growing and Ornamental Box Populations in Artvin, Turkey, Kastamonu Üniversitesi Orman Fakültesi Dergisi (2019) | DOI

[4] Averill, A. L.; Prokopy, R. J. Intraspecific Competition in the Tephritid Fruit Fly Rhagoletis Pomonella, Ecology, Volume 68 (1987) no. 4, pp. 878-886 | DOI

[5] Awmack, C. S.; Leather, S. R. Host Plant Quality and Fecundity in Herbivorous Insects, Annual Review of Entomology, Volume 47 (2002) no. 1, pp. 817-844 | DOI

[6] Barnes, E. E.; Murphy, S. M. Time-lagged intraspecific competition in temporally separated cohorts of a generalist insect, Oecologia, Volume 186 (2018) no. 3, pp. 711-718 | DOI

[7] Baur, B.; Jung, J.; Rusterholz, H. Defoliation of wild native box trees (Buxus sempervirens) : Does box rust (Puccinia buxi) infection influence herbivory, survival and growth of the invasive Cydalima perspectalis ?, Journal of Applied Entomology, Volume 143 (2019) no. 7, pp. 766-775 | DOI

[8] Benrey, B.; Denno, R. F. The Slow-Growth--High-Mortality Hypothesis: A Test Using the Cabbage Butterfly, Ecology, Volume 78 (1997) no. 4 | DOI

[9] Bergamini, L. L.; Almeida-Neto, M. Female Preference and Offspring Performance in the Seed Beetle Gibbobruchus bergamini Manfio & Ribeiro-Costa (Coleoptera: Chrysomelidae): A Multi-Scale Comparison, Neotropical Entomology, Volume 44 (2015) no. 4, pp. 328-337 | DOI

[10] Blenn, B.; Bandoly, M.; Küffner, A.; Otte, T.; Geiselhardt, S.; Fatouros, N. E.; Hilker, M. Insect Egg Deposition Induces Indirect Defense and Epicuticular Wax Changes in Arabidopsis thaliana, Journal of Chemical Ecology, Volume 38 (2012) no. 7, pp. 882-892 | DOI

[11] Bultman, T. L.; Faeth, S. H. Experimental Evidence for Intraspecific Competition in a Lepidopteran Leaf Miner, Ecology, Volume 67 (1986) no. 2, pp. 442-448 | DOI

[12] Burnham, K. P.; Anderson, D. R. Model selection and multimodel inference a practical information-theoretic approach, Springer, New York, 2002

[13] Colasurdo, N.; Gélinas, Y.; Despland, E. Larval nutrition affects life history traits in a capital breeding moth, Journal of Experimental Biology, Volume 212 (2009) no. 12, pp. 1794-1800 | DOI

[14] D. Coley, P.; L. Bateman, M.; A. Kursar, T. The effects of plant quality on caterpillar growth and defense against natural enemies, Oikos, Volume 115 (2006) no. 2, pp. 219-228 | DOI

[15] De Moraes, C. M.; Mescher, M. C.; Tumlinson, J. H. Caterpillar-induced nocturnal plant volatiles repel conspecific females, Nature, Volume 410 (2001) no. 6828, pp. 577-580 | DOI

[16] Denno, R. F.; McClure, M. S.; Ott, J. R. Interspecific Interactions in Phytophagous Insects: Competition Reexamined and Resurrected, Annual Review of Entomology, Volume 40 (1995) no. 1, pp. 297-331 | DOI

[17] Faeth, S. H. Indirect Interactions Between Temporally Separated Herbivores Mediated by the Host Plant, Ecology, Volume 67 (1986) no. 2, pp. 479-494 | DOI

[18] Faeth, S. H. Interspecific and Intraspecific Interactions Via Plant Responses to Folivory: An Experimental Field Test, Ecology, Volume 73 (1992) no. 5, pp. 1802-1813 | DOI

[19] Fatouros, N. E.; Lucas-Barbosa, D.; Weldegergis, B. T.; Pashalidou, F. G.; van Loon, J. J. A.; Dicke, M.; Harvey, J. A.; Gols, R.; Huigens, M. E. Plant Volatiles Induced by Herbivore Egg Deposition Affect Insects of Different Trophic Levels, PLoS ONE, Volume 7 (2012) no. 8 | DOI

[20] Fisher, D. N.; Haines, J. A.; Boutin, S.; Dantzer, B.; Lane, J. E.; Coltman, D. W.; McAdam, A. G. Indirect effects on fitness between individuals that have never met via an extended phenotype, Ecology Letters, Volume 22 (2019) no. 4, pp. 697-706 | DOI

[21] Fox, J.; Weisberg, S.; Adler, D.; Bates, D.; Baud-Bovy, G.; Ellison, S.; Firth, D.; Friendly, M.; Gorjanc, G.; Graves, S.; Heiberger, R.; Laboissiere, R.; Monette, G.; Murdoch, D.; Nilsson, H.; Ogle, D.; Ripley, B.; Venables, W.; Winsemius, D.; Zeileis, A.; R-Core, Car: Companion to Applied Regression, 2016

[22] P. Godinho, D.; Janssen, A.; Dias, T.; Cruz, C.; Magalhães, S. Down-regulation of plant defence in a resident spider mite species and its effect upon con- and heterospecifics, Oecologia, Volume 180 (2016) no. 1, pp. 161-167 | DOI

[23] Godinho, D. P.; Janssen, A.; Li, D.; Cruz, C.; Magalhães, S. The distribution of herbivores between leaves matches their performance only in the absence of competitors, Ecology and Evolution, Volume 10 (2020) no. 15, pp. 8405-8415 | DOI

[24] Gripenberg, S.; Mayhew, P. J.; Parnell, M.; Roslin, T. A meta-analysis of preference-performance relationships in phytophagous insects, Ecology Letters, Volume 13 (2010) no. 3, pp. 383-393 | DOI

[25] Hashem, M.; Ahmed, A.; Mohamed, S.; Sewify, G.; Khalil, S. Oviposition deterrent effect ofSpodoptera littoralis(Boisd.) larval frass to adult females of two major noctuid insect pests, Archives Of Phytopathology And Plant Protection, Volume 46 (2013) no. 8, pp. 911-916 | DOI

[26] Hilker, M.; Fatouros, N. E. Plant Responses to Insect Egg Deposition, Annual Review of Entomology, Volume 60 (2015) no. 1, pp. 493-515 | DOI

[27] Honěk, A.; Honek, A. Intraspecific Variation in Body Size and Fecundity in Insects: A General Relationship, Oikos, Volume 66 (1993) no. 3 | DOI

[28] Hopper, K. R. Risk-spreading and bet-hedging in insect population biology, Annual Review of Entomology, Volume 44 (1999) no. 1, pp. 535-560 | DOI

[29] Jactel, H.; Koricheva, J.; Castagneyrol, B. Responses of forest insect pests to climate change: not so simple, Current Opinion in Insect Science, Volume 35 (2019), pp. 103-108 | DOI

[30] Jones, T.; Finch, S. The effect of a chemical deterrent, released from the frass of caterpillars of the garden pebble moth, on cabbage root fly oviposition, Entomologia Experimentalis et Applicata, Volume 45 (1987) no. 3, pp. 283-288 | DOI

[31] Kaplan, I.; Denno, R. F. Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory, Ecology Letters, Volume 10 (2007) no. 10, pp. 977-994 | DOI

[32] Karban, R. The ecology and evolution of induced resistance against herbivores, Functional Ecology, Volume 25 (2011) no. 2, pp. 339-347 | DOI

[33] Kaygin, A. T.; Taşdeler, C. Cydalima perspectalis (Walker) (Lepidoptera: Crambidae, Spilomelinae)’in Türkiye’de Coğrafi Yayılışı, Yaşam Döngüsü Ve Zararı, Bartın Orman Fakültesi Dergisi, Volume 21 (2019) no. 3, pp. 833-847 | DOI

[34] Kenis, M.; Nacambo ,S., ; Leuthardt, F. L. G.; di Domenico, F.; Haye, T. The box tree moth, Cydalima perspectalis, in Europe: Horticultural pest or environmental disaster?, Aliens: The Invasive Species Bulletin (2013)

[35] Leuthardt, F. L. G.; Baur, B. Oviposition preference and larval development of the invasive moth Cydalima perspectalis on five European box-tree varieties, Journal of Applied Entomology, Volume 137 (2013) no. 6, pp. 437-444 | DOI

[36] Leuthardt, F. L. G.; Glauser, G.; Baur, B. Composition of alkaloids in different box tree varieties and their uptake by the box tree moth Cydalima perspectalis, Chemoecology, Volume 23 (2013) no. 4, pp. 203-212 | DOI

[37] Marchand, D.; McNeil, J. N. Avoidance of intraspecific competition via host modification in a grazing, fruit-eating insect, Animal Behaviour, Volume 67 (2004) no. 3, pp. 397-402 | DOI

[38] Martínez, G.; Finozzi, M. V.; Cantero, G.; Soler, R.; Dicke, M.; González, A. Oviposition preference but not adult feeding preference matches with offspring performance in the bronze bugThaumastocoris peregrinus, Entomologia Experimentalis et Applicata, Volume 163 (2017) no. 1, pp. 101-111 | DOI

[39] Matošević, D.; Lukić, I.; Bras, A.; Lacković, N.; Pernek, M. Spatial Distribution, Genetic Diversity and Food Choice of Box Tree Moth (Cydalima perspectalis) in Croatia, South-east European forestry, Volume 8 (2017) no. 1 | DOI

[40] Milanović, S.; Lazarević, J.; Popović, Z.; Miletić, Z.; Kostić, M.; Radulović, Z.; Karadžić, D.; Vuleta, A. Preference and performance of the larvae of Lymantria dispar (Lepidoptera: Lymantriidae) on three species of European oaks, European Journal of Entomology, Volume 111 (2014) no. 3, pp. 371-378 | DOI

[41] Molnár, B. P.; Tóth, Z.; Kárpáti, Z. Synthetic blend of larval frass volatiles repel oviposition in the invasive box tree moth, Cydalima perspectalis, Journal of Pest Science, Volume 90 (2017) no. 3, pp. 873-885 | DOI

[42] Moreau, J.; Benrey, B.; Thiery, D. Assessing larval food quality for phytophagous insects: are the facts as simple as they appear?, Functional Ecology, Volume 20 (2006) no. 4, pp. 592-600 | DOI

[43] Moreira, X.; Abdala-Roberts, L.; Castagneyrol, B. Interactions between plant defence signalling pathways: Evidence from bioassays with insect herbivores and plant pathogens, Journal of Ecology, Volume 106 (2018) no. 6, pp. 2353-2364 | DOI

[44] Moura, R. R.; Ribeiro, P. V. A.; Pereira, B. G.; Quero, A.; Carvalho, R. L.; Oliveira, D. C. Food, shelter or competitors? Overlapping of life stages and host plant selection in a Neotropical stink bug species, Journal of Plant Interactions, Volume 12 (2017) no. 1, pp. 560-566 | DOI

[45] Nykänen, H.; Koricheva, J. Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis, Oikos, Volume 104 (2004) no. 2, pp. 247-268 | DOI

[46] Pfennig, K. S.; Pfennig, D. W. Dead Spadefoot Tadpoles Adaptively Modify Development in Future Generations: A Novel Form of Nongenetic Inheritance?, Copeia, Volume 108 (2020) no. 1 | DOI

[47] Pinheiro, J.; Bates, D.; DebRoy, S.; Sarkar, D.; R Core Team, Nlme: Linear and Nonlinear Mixed Effects Models., 2020

[48] Poelman, E. H.; Broekgaarden, C.; Van Loon, J. J. A.; Dicke, M. Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field, Molecular Ecology, Volume 17 (2008) no. 14, pp. 3352-3365 | DOI

[49] Putten, W. H.; Bradford, M. A.; Pernilla Brinkman, E.; Voorde, T. F. J.; Veen, G. F. Where, when and how plant–soil feedback matters in a changing world, Functional Ecology, Volume 30 (2016) no. 7, pp. 1109-1121 | DOI

[50] Root, R. B.; Kareiva, P. M. The Search for Resources by Cabbage Butterflies (Pieris Rapae): Ecological Consequences and Adaptive Significance of Markovian Movements in a Patchy Environment, Ecology, Volume 65 (1984) no. 1, pp. 147-165 | DOI

[51] Sarmento, R. A.; Lemos, F.; Bleeker, P. M.; Schuurink, R. C.; Pallini, A.; Oliveira, M. G. A.; Lima, E. R.; Kant, M.; Sabelis, M. W.; Janssen, A. A herbivore that manipulates plant defence, Ecology Letters, Volume 14 (2011) no. 3, pp. 229-236 | DOI

[52] Sato, Y.; Yano, S.; Takabayashi, J.; Ohsaki, N. Pieris rapae (Ledidoptera : Pieridae) females avoid oviposition on Rorippa indica plants infested by conspecific larvae, Applied Entomology and Zoology, Volume 34 (1999) no. 3, pp. 333-337 | DOI

[53] Shiojiri, K.; Takabayashi, J. Effects of specialist parasitoids on oviposition preference of phytophagous insects: encounter-dilution effects in a tritrophic interaction, Ecological Entomology, Volume 28 (2003) no. 5, pp. 573-578 | DOI

[54] Simpson, S. J.; Simpson, C. L. The Mechanisms of Nutritional Compensation by Phytophagous Insects. Insect-Plant Interactions (1990): Volume II, CRC Press, 1990

[55] Stam, J. M.; Kroes, A.; Li, Y.; Gols, R.; van Loon, J. J.; Poelman, E. H.; Dicke, M. Plant Interactions with Multiple Insect Herbivores: From Community to Genes, Annual Review of Plant Biology, Volume 65 (2014) no. 1, pp. 689-713 | DOI

[56] Tammaru, T.; Haukioja, E. Capital Breeders and Income Breeders among Lepidoptera: Consequences to Population Dynamics, Oikos, Volume 77 (1996) no. 3 | DOI

[57] R Core Team, R: A language and environment for statistical computing, 2018

[58] Uesugi, A. The slow-growth high-mortality hypothesis: direct experimental support in a leafmining fly, Ecological Entomology, Volume 40 (2015) no. 3, pp. 221-228 | DOI

[59] Visakorpi, K.; Riutta, T.; Martínez‐Bauer, A. E.; Salminen, J.; Gripenberg, S. Insect community structure covaries with host plant chemistry but is not affected by prior herbivory, Ecology, Volume 100 (2019) no. 8 | DOI

[60] Wan, H.; Haye, T.; Kenis, M.; Nacambo, S.; Xu, H.; Zhang, F.; Li, H. Biology and natural enemies ofCydalima perspectalisin Asia: Is there biological control potential in Europe?, Journal of Applied Entomology, Volume 138 (2014) no. 10, pp. 715-722 | DOI

[61] Weeraddana, C. D. S.; Evenden, M. L. Herbivore‐induced plants do not affect oviposition but do affect fitness of subsequent herbivores on canola, Entomologia Experimentalis et Applicata, Volume 167 (2019) no. 4, pp. 341-349 | DOI

[62] Wise, M. J.; Weinberg, A. M. Prior flea beetle herbivory affects oviposition preference and larval performance of a potato beetle on their shared host plant, Ecological Entomology, Volume 27 (2002) no. 1, pp. 115-122 | DOI

[63] WRATTEN, S. D.; EDWARDS, P. J.; WINDER, L. Insect herbivory in relation to dynamic changes in host plant quality*, Biological Journal of the Linnean Society, Volume 35 (1988) no. 4, pp. 339-350 | DOI

[64] Zuur, A. F.; Ieno, E. N.; Walker, N.; Saveliev, A. A.; Smith, G. M. Mixed effects models and extensions in ecology with R, Statistics for Biology and Health, Springer New York, New York, NY, 2009 | DOI

Cited by Sources: